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Auberjonois was born in New York City on 1 June 1940. His father, Fernand Auberjonois, was a journalist, and his grandfather, also called René Auberjonois, a Swiss painter. His mother was Princess Laure Murat, who was descended from Joachim Murat, one of Napoleon Bonaparte's marshals, and husband of Caroline Bonaparte, Napoleon's youngest sister.

Actor Armin Shimerman, who played Quark on DS9, was and remains a close friend of Auberjonois. They acted in a play together prior to DS9 and spent many hours together in make-up chairs while starring in DS9.

Auberjonois initially disliked DS9's season three premiere, "The Search, Part I", in which his orphan character, Odo, met his people, the Founders, for the first time and discovered his origin. Auberjonois felt part of Odo's mystery and vitality as a character stemmed from his not knowing where he came from. However, Auberjonois soon came to like the development because new twists were added as more was learned about Odo's past – whether Odo's loyalties would reside with the Founders and leaders of the Dominion or with the Federation, and whether others would trust Odo during the Dominion War added complexity to his character even after his origin was established. (DS9 DVD Season 3 special features)

Auberjonois has been performing on the Broadway stage since the late 1960s, beginning with a revival of William Shakespeare's King Lear and a play called A Cry of Players as part of the Repertory Theatre of Lincoln Center. Both productions ran from November 1968 through February 1969 with a total of 72 performances each; on A Cry of Players, he co-starred with Frank Langella, who later guest-starred on DS9.

In 1970, Auberjonois won a Tony Award as Best Featured Actor in for his portrayal of Sebastian Baye in Coco, which ran from 18 December 1969 through 3 October 1970. In 1972, Auberjonois co-starred with Stephen McHattie in a production of Shakespeare's Twelfth Night.

Auberjonois received a second Tony Award nomination in 1974 for his role in The Good Doctor (opposite Christopher Plummer) and a third nomination in 1985 for playing The Duke in Big River. He also won a Drama Desk Award as Outstanding Featured Actor in a Musical for Big River. Auberjonois performed in Big River from its premiere on 25 April 1985 until 2 September of that year, when his role as The Duke was recast. By 8 October, future Star Trek: The Next Generation star Brent Spiner had taken over the role which Auberjonois had originated; in January 1986, the role of The Duke went to TNG guest actor Ken Jenkins. Another TNG guest actor, Bob Gunton, played the role of The King in Big River during both Auberjonois' and Spiner's tenures.

Auberjonois received yet another Tony Award nomination, as well as a Drama Desk nomination, for his dual role in the musical comedy City of Angels, which ran from 1989 through 1992. Auberjonois most recently starred on Broadway in Dance of the Vampires from December 2002 through January 2003 and Sly Fox in 2004. In 2007, he again appeared onstage with Frank Langella (who won a Tony for his performance as the former President) in the widely acclaimed drama Frost/Nixon.

Auberjonois first gained fame on television for his Emmy Award-nominated role as the snooty Clayton Endicott III on the comedy series Benson. Auberjonois joined the cast of Benson at the start of its second season in 1980 and remained with the series until its end in 1986. One of his co-stars was Ethan Phillips (Neelix of Star Trek: Voyager), who joined the show's cast at the same time but left before the final season.

Between 2004 and 2008, Auberjonois appeared alongside TOS star William Shatner in the ABC series Boston Legal. In this series, Auberjonois played Paul Lewiston, who was the managing partner of law firm Crane, Poole & Schmidt for the first three seasons. He was credited as a guest star when the series began in October 2004 but he officially became a regular halfway through the first season. In June 2007, however, it was announced that Auberjonois would no longer be a regular beginning with the show's fourth season. Auberjonois' character was replaced in the next season by Carl Sack, played by Star Trek III: The Search for Spock actor John Larroquette.

Auberjonois' friend and fellow DS9 star Armin Shimerman had a recurring role on the series. Shimerman played a judge who is an acquaintance of Auberjonois' character – and who is suspected of being involved in the murder of Shimerman's wife. Although the two did not act together during the first three of Shimerman's seven episodes, they finally shared a scene together in the fourth episode, entitled "Desperately Seeking Shirley". Voyager actor and Auberjonois' Benson co-star Ethan Phillips also appeared on Boston Legal during this time, playing the father of the boy accused of killing Shimerman's wife.

After being ousted as a regular, Auberjonois returned to the series as a special guest star on four occasions, where it is learned his character has moved up to a higher floor at the firm. He appeared in one episode of the show's fourth season, entitled "Oral Contracts," in 2007; Steven Culp and recurring Boston Legal actor Henry Gibson also guest-starred in this episode. Auberjonois made another appearance in the seventh episode of the show's fifth and final season, titled "Mad Cows," in which Steven Anderson, Henry Gibson, and Ned Vaughn also appeared. Auberjonois was then brought back for the last two episodes of the series, "Made in China" and "Last Call," which were aired together as a two-hour series finale on 8 December 2008.

Between 2000 and 2002, Auberjonois guest-starred in two episodes of The Practice, receiving his second Emmy nomination (after Benson) for his first appearance on the show. Boston Legal, in which Auberjonois later starred, is a spinoff of The Practice, although he did not play the same character.

Auberjonois attended the Comedy Central Roast of William Shatner in August 2006, where his Boston Legal co-star and fellow Trek actor was subjected to the whims of stand-up comics. Also in the audience were Jeri Ryan of Voyager fame (who guest-starred on Boston Legal) and Brent Spiner from TNG. Shatner's TOS cohorts Nichelle Nichols and George Takei participated in the roast, as did Voyager guest star Andy Dick, while Clint Howard and Sarah Silverman had recorded messages to Shatner (Howard appeared in character as an alcoholic Balok, addicted to tranya). The event was hosted by Jason Alexander.

In 2010 Auberjonois became the first former Star Trek star to be a guest star on the Syfy series Warehouse 13. In the episode he played Hugo Miller, a former warehouse employee who accidentally downloaded half of his mind into an experimental computer system. At the end of the episode his character, with his mind whole again, was offered a job by another visiting guest, Douglas Fargo (Neil Grayston) from Syfy's Eureka. He has yet to make an appearance on that series.

Auberjonois and Schuck went on to co-star together in Altman's McCabe & Mrs. Miller in 1971, while Auberjonois himself starred in Altman's Images the following year. Auberjonois and Kellerman went on to co-star together in 1976's The Big Bus, along with Vic Tayback. This film, however, was not directed by Robert Altman. Auberjonois and John Schuck also co-starred together in the 1971 made-for-TV movie Once Upon a Dead Man.

Interestingly, Auberjonois lent his voice to an animated series called Wildfire in 1986, which revolved around a horse. His DS9 co-star, Nana Visitor, starred in a live-action TV series called Wildfire in 2005 – which is also about a horse.

Along with Kenneth Messeroll and Christopher Collins, Auberjonois was one of the uncredited voice actors for Star Blazers. He was the voice of Sandor for its third season, The Bolar Wars.

Auberjonois is one of only five actors to have appeared in both Batman: The Animated Series and a live-action movie based on the Batman comics franchise - the others being Ed Begley, Jr., John Glover, Vincent Schiavelli, and U.S. Senator Patrick Leahy.

He also had an uncredited voice-over role in the live-action Disney movie The Princess Diaries. In 2005, he voiced the character known as Mr. Sneaps in Geppetto's Secret. Armin Shimerman; DS9's Quark, voices a character in that production, as well. In 2005, he also provided the English voice for a character in the Studio Ghibli anime feature Neko no Ongaeshi (The Cat Returns) (with additional voices by Bradley Pierce).